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Abbreviation (ISO4): Prog Chem      Editor in chief: Jincai ZHAO

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Progress in Chemistry >

2024 , Vol. 36 >Issue 6: 815 - 826

DOI: https://doi.org/10.7536/PC231113

Review

Construction of Polymer-Microorganism Hybrids for Catalysis

  • Yutai Zou 1, 2 ,
  • Wenshuo Wang , 2, * ,
  • Jian Liu , 1, 2, *
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  • 1 College of Materials Science and Engineering, Qingdao University of Science and Technology, Qingdao 266042, China
  • 2 Key Laboratory of Photoelectric Conversion and Utilization of Solar Energy, Qingdao New Energy Shandong Laboratory, Qingdao Institute of Bioenergy and Bioprocess, Chinese Academy of Sciences, Qingdao 266101, China
* e-mail: (Wenshuo Wang);
(Jian Liu)

Received date: 2023-11-21

  Revised date: 2024-01-03

  Online published: 2024-03-15

Supported by

National Natural Science Foundation of China(22175104)

National Natural Science Foundation of China(22205253)

Natural Science Foundation of Shandong Province(ZR2019ZD47)

Shandong Excellent Young Scientists Fund Program(2023HWYQ-105)

Taishan Scholars Program

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Abstract

The design and development of material-microorganism hybrid systems that can use solar energy for green biosynthesis is expected to provide human society with a viable solution for addressing the global energy shortage and environmental crisis.in recent years,the construction of hybrid systems by coupling excellent physical and chemical features of artificial materials with the biosynthetic function of microorganisms has received extensive attention.polymeric materials,due to versatile functions,excellent designability and good biocompatibility,have been widely used to construct material-microorganism hybrid systems,and have shown broad application prospects In the field of bioenergy.Based on the functional features of Polymeric materials,this paper systematically summarizes different types of polymer-microorganism biohybrid systems,and discusses the augmentation of their catalytic performance by enhancing light utilization,accelerating electron transfer,and stabilizing biological activity.Finally,the challenges and future development of polymer-microorganism hybrid systems are discussed.

Contents

1 Introduction

2 Construction of polymer-microorganism biohybrids

2.1 Conjugated polymers

2.2 Polyelectrolytes and polyphenols

3 Polymer-microorganism biohybrids with enhanced biocatalysis

3.1 Enhance light utilization to strengthen microbial photosynthesis

3.2 Accelerate electron transfer to strengthen microbial electrosynthesis

3.3 Stabilize cell activity to strengthen microbial conversion of chemicals

4 Conclusion and outlook

Key words： polymer; biohybrid; biocatalysis; cell surface engineering; semi-artificial photosynthesis

Cite this article

Yutai Zou , Wenshuo Wang , Jian Liu . Construction of Polymer-Microorganism Hybrids for Catalysis[J]. Progress in Chemistry, 2024 , 36(6) : 815 -826 . DOI: 10.7536/PC231113

1 Introduction

Large-scale development and utilization of green renewable energy to replace fossil fuels such as coal,oil and natural gas is an important measure to solve the energy and environmental crisis facing human society.Converting renewable energy such as solar energy,wind energy,water energy and other green energy into electricity can provide sustainable power for industrial production and human activities.However,renewable energy has the characteristics of volatility and intermittency,and its large-scale application also depends on the development of energy storage technology.In nature,plants and photosynthetic microorganisms convert water（H2O）and carbon dioxide（CO2）into oxygen（O2）and organic matter through photosynthesis,and store solar energy in the form of chemical energy,which constitutes the basis of all life activities on the earth[1]。 Green synthesis to produce high-value chemicals and fuels using renewable energy such as solar energy by simulating photosynthesis has attracted wide interest from both academia and industry。
In the past few decades,various catalytic systems such as photocatalysis,electrocatalysis and biocatalysis have been widely studied to realize the conversion of energy and matter[2⇓~4][5⇓~7][8⇓~10]。 However,photocatalysis and electrocatalysis have the problems of poor reaction specificity and low energy conversion efficiency,which make it difficult to meet the current demand for the production of high-value chemicals.Enzyme-based microbial catalytic system can convert air components into high-value products,and can also catalyze the conversion of specific organic compounds,and has the advantages of mild reaction conditions,high reaction specificity,designable synthetic routes,and self-replication of biocatalysts,which provides a strong guarantee for green synthesis[11⇓~13]。 Microorganisms can reduce the catalytic energy barrier through the specific structure and coordination environment of enzymes,and achieve mild,efficient and highly specific catalytic reaction process[14,15]。 At the same time,different enzymes in microbial cells cooperate to form a delicate metabolic pathway,which uses air components such as inorganic small molecules such as CO2,nitrogen（N2）,H2O and organic macromolecules such as biomass to synthesize various high-value chemicals,fuels and functional materials accurately and efficiently,which is incomparable to chemical catalysis[12,16,17]。 For example,the photoautotrophic microorganism Synechococcus cyanobacteria can convert solar energy into chemical energy to fix CO2through the Calvin cycle,which can be combined with genetic engineering to produce chemicals such as isobutyraldehyde[18]; The chemoautotrophic microorganism Clostridium autoalcoholicum can use carbon monoxide and hydrogen as electron donors,fix CO2through the reduced acetyl-Coa pathway,and produce chemicals such as acetone and isopropanol on a large scale[19]; Heterotrophic microbial yeasts can be engineered to convert sugar molecules into artemisinic acid,a precursor of antimalarial drugs[20]。
In recent years,people have begun to couple the ingenious Synthetic functions of microorganisms with the excellent characteristics of synthetic materials,and construct a variety of material-microbial hybrid systems to achieve more efficient catalytic transformation by combining the advantages of both.synthetic materials,including photocatalytic materials such as cadmium sulfide,indium phosphide,Poly(fluorene phenylene)(PFP),conductive materials such as silver nanoparticles,iron sulfide,Polypyrrole(PPy),and other functional materials such as silicon dioxide,calcium carbonate,Polydopamine(PDA),are widely used to couple microorganisms to enhance their catalytic performance[21⇓⇓⇓⇓~26][27⇓⇓~30][31⇓⇓⇓~35]。 Polymers are high molecular weight compounds formed by chemical bonding of small molecular repeating units,which are widely used in the construction of material-microbial hybrids because of their diverse functions,strong designability,and easy binding with cells[26,33]。 Polymer materials also have extensive research in cell engineering,For example,they can be integrated with bacteria,fungi,microalgae,animal cells,etc.for cell surface engineering or internal functionalization[36][37⇓⇓~40]。 In addition,the grafted polymer can also serve as an interface between cells and other functional nanomaterials to further guide biomineralization,assist metal deposition,and fuse other materials such as indium phosphide nanoparticles[41][42][43]。 Therefore,the cell engineering guided by polymer materials is highly operable and designable,which can be used to develop functional materials and biological hybrid systems,and has broad application prospects in the fields of biomedicine,bioelectronics and bioenergy[32,44⇓~46]。 In polymer-microbial hybrid systems,photoactive polymers,conductive polymers and other functional polymers can enhance the catalytic performance of the hybrid through excellent photoelectric properties and providing a protective coating for microorganisms.The semi-artificial photosynthetic system in which microorganisms are hybridized with photoactive polymers can use photogenerated electrons as a mediator to provide reducing power and improve the biotransformation efficiency of CO2[47⇓~49]。 the hybrid microbial electrosynthesis system of microorganisms and conducting polymers can accelerate the transfer rate of electrons between microbial cells and electrodes,and improve the biosynthetic performance[50]。 in addition,the coating of polydopamine on the surface of microorganisms can provide physical and chemical protection for them and improve the stability of biocatalysts In complex catalytic environments[51,52]。
in this paper,the construction and catalytic application of polymer-microorganism hybrid system were systematically summarized.First of all,this paper outlines the construction of several different types of hybrids according to the properties and functions of polymer materials.Secondly,the improvement of biocatalytic performance in polymer-microorganism hybrid system was reviewed in detail from three aspects:enhancing light energy utilization,accelerating electron transfer,and stabilizing bioactivity(Fig.1).Finally,the future research of polymer-microbial hybrids in catalysis is prospected。
图1 聚合物-微生物杂合体的构建与催化应用

Fig. 1 The construction of polymer-microorganism biohybrids for catalysis

2 Construction of polymer-microbial hybrids.

polymer-microorganism hybrids use light energy,electric energy,chemical energy and reducing power for biocatalysis,which has great advantages and development potential in the green synthesis of high-value chemicals.Different types of Polymers(including ionic polyelectrolytes,polyphenolic polymers and conjugated polymers)can be combined with microorganisms to form polymer-microorganism hybrids through electrostatic interaction,hydrophobic interaction,in-situ polymerization or assembly.polymers play a role in harvesting light,conducting electricity,stabilizing microorganisms,and mediating the coupling of microorganisms with other functional materials.the construction of polymer-microorganism hybrids will be described separately according to the type of polymer in this section。

2.1 Conjugated polymer

Conjugated polymers exhibit excellent optoelectronic properties due to the energy band gap caused by delocalizedπbonds[53]。 Conjugated polymers are ideal materials for coupling photosynthetic and electrical microorganisms because of their adjustable optical band gap,efficient electron transfer ability and good biocompatibility[54]。 the constructed conjugated polymer-microorganism hybrid can improve the utilization rate of light energy and accelerate electron transfer,and enhance the biosynthetic performance driven by light and electricity by injecting additional electrons into the microbial metabolic pathway。
Photoactive conjugated polymers such as Poly(boron-dipyrromethene-co-fluorene)(PBF),PFP,Poly(p-phenylene vinylene),and carbon nitride have been reported to bind to various microbial cells to construct semi-artificial photosynthetic systems[55][47⇓~49][56][57⇓⇓~60]。 For example,Zhang Zhonghai et al.Reported the construction of a hybrid system by endocytosis of carbon nitride quantum dots by Escherichia coli to achieve efficient solar hydrogen production[61]。 conducting conjugated polymers such as PPy,p(cNDI-gT2),PFP,PDA,etc.Are used as Conducting materials in bioelectrochemical systems,which can improve the electron transfer between microorganisms and electrodes and thus enhance the biocatalytic efficiency[29][50][62][28]。 For example,PPy-encapsulated acetogens can improve microbial electrosynthesis performance through enhanced electron transfer[63]。 PFP or p(cNDI-gT2)showed enhanced bidirectional electron transfer ability after binding to Shewanella[50,62]。 In addition to transferring electrons on the electrodes,conducting polymers are also used to facilitate the transfer of photoexcited electrons.Huang Xin et al.Constructed an abiotic shell on the surface of photosynthetic microorganism Chlorella vulgaris,including an ultrathin iron ion doped PPy inner layer and a calcium carbonate outer layer[33]。 The polymer layer can consume O2to shape an anoxic environment,thereby activating hydrogenase activity for biological hydrogen production.PPy is used as a conductive medium to capture and transport extracellular electrons into Chlorella cells,thereby increasing the rate of hydrogen production 。
conjugated polymers can bind to microorganisms through electrostatic interactions,hydrophobic interactions,in situ polymerization,or assembly(Fig.2).By introducing quaternary ammonium salt groups into the side chain,the conjugated polymer not only has enhanced water solubility,but also can be combined with electronegative microorganisms through electrostatic interaction.At the same time,the hydrophobic carbon chain of the conjugated polymer can be inserted into the cell membrane to further enhance the transfer of photogenerated electrons into the cell。
图2 共轭聚合物与微生物结合用于构建生物杂合体：（1）共轭聚合物通过静电相互作用和疏水相互作用结合在微生物表面；（2）共轭聚合物通过原位聚合结合在微生物表面；（3）聚合物量子点等纳米结构的共轭聚合物结合在微生物表面

Fig. 2 The construction of biohybrids through the combination of the conjugated polymer (CP) with the microorganism. (1) The combination of the CP with the microorganism through electrostatic interaction and hydrophobic interaction. (2) The combination of the CP with the microorganism through in situ polymerization. (3) The combination of the CP nanoparticles such as polymer dots with the microorganism

In addition to chain molecules,conjugated polymer nanoparticles have also been used to couple microorganisms.Water-soluble conjugated polymer nanoparticles prepared by coprecipitation were used to bind microorganisms such as Rhodopseudomonas palustris,Ralstonia,and engineered Escherichia coli[64][65][66]。 conjugated polymers can also be directly grown on microbial surfaces by means of in situ polymerization.Wang et al.Realized the combination of Conjugated polymer and cells by using biological palladium-catalyzed Sonagashira polymerization[56]。 in this report,the researchers first used electrostatic interactions to bind palladium ions on the surface of Chlorella,and then molybdase and sodium formate reductant reduced the palladium ions to biological palladium catalyst.Subsequently,the added cationic monomer was subjected to Sonagashira polymerization in the presence of biopalladium catalyst,and the conjugated polymer was generated in situ on the surface of Chlorella.PPy and PDA can also be assembled on the surface of microbial cells in situ by monomer oxidative polymerization[29][28,67]。
Photoactive conjugated polymers can be used as artificial antennas to compensate for the lack of light absorption by natural pigments of photosynthetic microorganisms,expand the range of photosynthetically active radiation,and improve photosynthetic efficiency[68]。 At the same time,photoactive polymers can enable non-photosynthetic microorganisms to use light energy to enhance biological metabolism and biosynthesis through photogenerated electron transfer[47,49]。 Conductive conjugated polymers can enhance the electron transfer between microorganisms and electrodes,which is helpful for electroactive microorganisms to improve their bioelectrochemical performance[29,50]。 Among them,the conductive polymer can enhance the efficiency of the utilization of cathode electrons by electrical microorganisms in the microbial electrosynthesis system,thereby improving the biosynthetic capacity[50]。 Therefore,it is of great significance to select appropriate conjugated polymers to construct polymer-microbial hybrid semi-artificial photosynthesis system and microbial electrosynthesis system,which can realize the conversion of energy and matter and then store renewable energy such as solar energy in the form of chemical energy。

2.2 Polyelectrolyte and polyphenolic polymer

in addition to conjugated polymers that enhance light absorption and electron transfer,polyelectrolytes and polyphenols are combined with microorganisms through electrostatic interaction and In situ assembly,which can not only serve as protective coatings on the surface of microorganisms to create a stable and controllable microenvironment for microbial catalytic synthesis,but also serve as interface layers to integrate other functional materials(Figure 3).In order to adapt to the surrounding environment,organisms in nature have evolved mineralized skeletons or other shells to isolate and protect themselves from harsh environments such as heat,radiation and chemicals[69,70]。 Inspired by this,polymer-based surface coating and biomimetic mineralization technology have been used to encapsulate cells to provide physical and chemical protection[71,72]。
图3 聚电解质和多酚类聚合物与微生物结合用于构建生物杂合体：（1）聚电解质通过静电相互作用结合在微生物表面；（2）多酚类聚合物通过原位聚合和配位作用组装在微生物表面；（3）聚合物在细胞表面集成其他功能材料如无机纳米颗粒或生物酶

Fig. 3 The construction of biohybrids through the combination of the polyelectrolytes and polyphenols with the microorganism. (1) The combination of polyelectrolytes with the microorganism through electrostatic interaction. (2) The assembly of polyphenols on the microorganism through in situ polymerization or coordination. (3) The integration of other functional materials such as inorganic nanoparticles or biological enzymes on the microorganism

polyelectrolytes are widely used in cell surface engineering studies.Because the membrane surface of microbial cells is electronegative,it can be electrostatically bound to microorganisms through electropositive polymers.Ionic Polyelectrolytes with opposite charges,such as Poly(diallyl-dimethylammonium chloride)(PDADMAC)and Polystyrene sulfonic acid(PSS),can be bound to the surface of microorganisms through electrostatic layer-by-layer self-assembly,and then biomimetic mineralization can be catalyzed by cationic polymers[31,73]。 At the same time,because polymers can carry different charges,materials carrying opposite charges such as silica particles or magnetic particles can be assembled on the surface of microbial cells through electrostatic interaction[34]。 Due to their physical and chemical protective effects,microbial catalysts encapsulated by polyelectrolytes and biomimetic mineralization show stable catalytic activity in complex catalytic systems.surface coating can also change the microenvironment of microorganisms and thus change their metabolic pathways.For example,polymer combined with surface display technology and biomimetic mineralization technology,integrated cadmium sulfide semiconductor nanoparticles and encapsulated silica shell on the surface of E.coli cells expressing oxygen-tolerant[nickel iron]-hydrogenase,realized a biohybrid system capable of hydrogen production under aerobic conditions[74]。 In addition,the magnetic particle modification can realize the manipulation and collection of microorganisms,which can be used for the recovery of petroleum after degradation and biocatalysis[75]。
Polyphenolic compounds such as dopamine and tannic acid are assembled on the surface of microbial cells in situ through the formation of hydrogen bonds,cation-πinteractions,ion complexation,etc.,and can also act as an interface layer to adhere to other functional materials to provide protection for microorganisms and shape the microbial catalytic microenvironment[76][77]。 For example,the PDA-modified microbial catalyst can stably carry out the catalytic reaction at the oil-water emulsion interface[52]。 the light-driven production of fine chemicals can be achieved by integrating the assembly of indium phosphide semiconductor nanoparticles onto the engineered yeast surface to construct a biohybrid system through tannic acid[43]。 in addition,Huang Xin et al.Constructed a sandwich structure around green algae through the sequential self-assembly of dopamine,laccase and tannic acid,In which laccase consumes oxygen produced by photosynthesis of green algae cells by catalyzing tannic acid oxidation.An anoxic microenvironment is formed on the surface of the green algae,and then the activation of hydrogenase is induced,so that the encapsulated cells are converted from photosynthetic oxygen production to hydrogen production[32]。
Ionic polyelectrolytes and polyphenolic polymers can be used as an interface layer to integrate other functional materials such as photocatalysts,conductive materials,magnetic particles,biological enzymes and so on on the cell surface,so that the polymer-microorganism hybrid system has more extensive and controllable functions.Among them,polymers or other materials introduced by polymers can provide mechanical skeleton and chemical protection for microorganisms,so that they can maintain long-term biological activity and stability In complex catalytic environment.in a word,the construction of polymer-microbial hybrids by using polymers to coat the surface of microbial cells can provide assistance for chemical transformation involving microorganisms under complex conditions。

3 Polymer-microbial hybrid enhanced biocatalysis

the production of fuels,chemicals and functional materials by microbial catalysis can convert green renewable energy into chemical energy for storage and provide various material products for human production and life,which provides a new way to solve the energy challenges and environmental problems caused by the excessive consumption of global fossil fuels.However,the pre-established synthetic pathways of microorganisms,which are preferentially used for cell growth and metabolism to maintain normal viability,can reduce the expected biosynthetic efficiency.by integrating the functional properties of synthetic polymers and the catalytic mechanism of naturally evolved enzymes in microorganisms,polymer-microorganism hybrids can use exogenous electrons and energy or stabilize the activity of microorganisms to enhance biocatalytic ability.At present,a variety of polymer-microbial hybrid systems have been developed and microbially catalyzed synthesis driven by light,electricity or chemical energy has been realized。

3.1 Enhancing Light Utilization and Microbial Photosynthesis

In nature,photosynthetic microorganisms capture sunlight for photosynthesis and convert H2O and CO2into O2and carbohydrates through light and dark reactions.Light absorption is the driving force and premise of photosynthesis,but the photosynthetically active radiation of 400~700 nm only accounts for 48.7%of the incident solar energy,and the energy conversion efficiency of photosynthetic microorganisms in nature is only about 1%,which is far below the theoretical maximum of microalgae and plants(about 12%and 6% )[78]。 Using photoactive polymers to expand the range of photosynthetically active radiation,photosynthetic microorganisms can absorb more photons in the light reaction stage and synthesize more nicotinamide adenine dinucleotide(NADPH)and adenosine triphosphate(ATP)to enhance the fixation and transformation of CO2in the dark reaction stage.In addition,light-driven biosynthesis can be achieved by injecting electrons generated by photoexcitation into non-photosynthetic microbial metabolic pathways[47,65]。
Wang et al.Constructed a series of conjugated polymer-photosynthetic microbial hybrids through electrostatic and hydrophobic interactions[55]。 For example,PBF-Chlorella pyrenoidosa hybrids can use PBF to regulate the state transition of photosystem II(PSII)and photosystem I(PSI)of Chlorella and enhance photosynthesis(Fig.4A).During the photoreaction of photosynthesis,PBF increased the production of O2,ATP and NADPH by 120%,97%and 76%,respectively.During the dark reaction,PBF increased the activity of ribulose-1,5-bisphosphate carboxylase by 1.5 times and the expression levels of RbcL and prk,which encode the enzymes required for carbon fixation,by 2.6 and 1.5 times,respectively.PFP-cyanobacteria(Synechococcus sp.PCC7942)hybrid can use the ultraviolet absorption characteristics of PFP to expand the spectral absorption range of cyanobacteria,improve light energy utilization and electron transport rate,and increase light reaction products[48]。 PFP enhanced the production of cyanobacterial O2,NADPH and ATP by 52.6%,47.9%and 27.2%,respectively.At the same time,the poly(p-phenylene ethynylene)-Chlorella hybrid constructed by in situ polymerization strategy uses the former to enhance blue light absorption and red light emission and accelerate PSI cycle electron transfer to improve ATP synthesis[56]。 Xing Chengfen et al.Coated CPNs-TAT on the surface of photosynthetic bacteria Rhodopseudomonas palustris to construct polymer-microorganism hybrid[64]。 CPNs-TAT in that hybrid convert ultraviolet light into visible light that can be absorbed by the bacteria to promote ATP synthesis and enhance bacterial photosynthesis.Therefore,through the construction of photoactive polymer-photosynthetic microbial hybrids,the use of polymers to expand the range of photosynthetically active radiation can effectively improve the metabolic activity of organisms。
图4 光活性聚合物增强微生物光能利用：（a）PBF-小球藻杂合体显示增强的光反应活性[55]；（b）PDI/PFP-热醋穆尔氏菌杂合体进行光驱动CO2还原产乙酸[47]；（c）PFP集成的多生物共生体利用CO2和N2进行光驱动γ-PGA生物合成[26]

Fig. 4 Photoactive polymers for enhanced microbial utilization of light. (a) PBF-Chlorella pyrenoidosa biohybrid with enhanced activity in light reaction of photosynthesis[55]; Copyright 2020, Science. (b) PDI/PFP-Moorella thermoacetica biohybrid for solar-driven CO2 reduction to acetic acid[47]; Copyright 2020, Wiley-VCH. (c) PFP-integrated multi-organism symbiont for solar-powered γ-PGA biosynthesis by utilizing CO2 and N2[26]. Copyright 2020, Science

The fixation and transformation of CO2through microbial metabolic pathways is of great significance to alleviate the energy and environmental crisis.Wang et al.Reported a hybrid constructed by conjugated polymer and non-photosynthetic bacteria Moorella thermoacetica,which can use light energy to achieve efficient CO2reduction for acetic acid production(Fig.4B )[47]。 In this work,perylene diimine derivative(PDI)and PFP were used as photosensitizers coated on the surface of bacteria,and the p-n heterojunction PFP/PDI layer formed had high electron/hole separation efficiency.Moorea thermoacetata can obtain photoexcited electrons from the PFP/PDI heterojunction,which drives the conversion of CO2to acetic acid through the Wood-Ljungdahl pathway,achieving a light utilization rate of 1.6%.Wang et al.Used biocompatible organic semiconductor polymer dots(Pdots)as photosensitizer to construct a hybrid system with Ralstonia eutropha H16 and electron shuttle medium neutral red[65]。 The photoelectrons generated by Pdots promote NADPH regeneration in bacteria through neutral red,and then drive the conversion of CO2to polyhydroxybutyrate through Calvin cycle,with a yield of(21.3±3.78)mg/L,which is nearly three times higher.Xiong et al.Designed a hybrid biophotocatalytic system by assembling Methanosarcina barkeri and carbon dot-functionalized polymeric carbon nitride(CDPCN )[59]。 Among them,CDPCN is used for microplastic photooxidation,and microorganisms are used for CO2photoreduction to produce methane,while using photogenerated holes and electrons.The system achieved nearly 100%selective conversion within 24 H.Therefore,by constructing photoactive polymer-microbial hybrids,the performance of non-photosynthetic microorganisms for carbon sequestration and production of high-value chemicals can be effectively improved by using photoelectrons generated by polymers 。
The conversion of N2currently relies on the Haber-Bosch process,which requires high-temperature and high-pressure reaction conditions and H2from fossil fuels.Therefore,the development of green biological nitrogen fixation technology with mild reaction conditions has important application prospects[79]。 Wang et al.Constructed a polymer-microorganism hybrid through the electrostatic interaction between cationic conjugated polymer PFP and Azotobacter Chroococcum to study nitrogen fixation,and enhanced the biological nitrogen fixation ability by improving the nitrogenase activity in Azotobacter Chroococcum[49]。 Under light irradiation,PFP enhanced nitrogenase activity,NH4+and amino acid production by 260%,44%and 47%,respectively,due to the promotion of electron transfer from redox proteins to cells.However,the slow autotrophic metabolism of a single strain limits the rate of nitrogen fixation,and the ammonia synthesized is more easily consumed by the bacteria themselves and converted into biomass.Therefore,Wang et al.Developed a multi-organism symbiont by co-hybridization of PFP and a variety of microorganisms,using CO2and N2in the air as carbon and nitrogen sources to selectively synthesize functional polypeptideγ-polyglutamic acid(γ-PGA)and antibiotic bacitracin A(Figure 4C )[26]。 In the symbiont,cyanobacteria perform CO2fixation,Rhodopseudomonas palustris perform N2fixation,Bacillus licheniformis perform target product biosynthesis,and the positively charged PFP brings the three microorganisms together to form a conductive network that facilitates direct interspecies electron transfer.At the same time,PFP enhances the photosynthesis of cyanobacteria and Rhodopseudomonas palustris through excellent light-harvesting performance,and promotes the fixation of CO2and N2.Finally,this modular design and the interspecies mutually beneficial relationship increased the synthesis rate ofγ-PGA by 104%to 144.2 mg/L 。
through the hybridization of the photoactive polymer and the microorganism,the polymer can use light energy to provide additional energy for the microorganism to improve the biological metabolic activity and biosynthesis ability,and realize efficient biological carbon fixation and biological nitrogen fixation.By genetic engineering and metabolic regulation of microorganisms,various types of microorganisms can synthesize various fuels,chemicals and functional materials Through different metabolic pathways such as Calvin cycle and Wood-Ljungdahl pathway[19,22,80,81]。

3.2 Accelerated Electron Transport Enhanced Microbial Electrosynthesis

Through extracellular electron transfer(EET),electroactive microorganisms transfer electrons generated in metabolic processes to Extracellular electron acceptors or receive electrons from Extracellular electron donors to maintain metabolic activities[82]。 Electrons can be transferred directly through redox proteins(such as cytochromes,flavoproteins,and cuprohemes)or through fimbriae and"nanowires",or indirectly through redox-active electron mediators(such as riboflavin,phenazines,and quinones)[82]。 In microbial electrochemical systems,the direction of EET is different when microorganisms act as anode and cathode.Among them,microorganisms as cathodes can use electrical energy to produce high-value chemicals by microbial electrosynthesis,which has important research and application value[83,84]。
Increasing the EET rate is the key to optimizing microbial electrosynthesis[85⇓~87]。 Reducing the interfacial electron transfer resistance by modifying the surface of bacteria with conductive polymers is an effective means to improve EET.Zeng Cuiping et al.Wrapped the highly conductive polymer PPy on the surface of acetogenic bacteria as the cathode of the electrolytic cell,successfully reduced the cathode resistance of the microbial electrosynthesis system by 33%-70%,and increased the acetate yield and Faradaic efficiency of the biocathode by 3-6 times[63]。 Li Zhengping et al.Studied conjugated polymer enhanced bidirectional EET and found that PFP not only has excellent electron transport ability,but also can enhance bidirectional EET by embedding into bacterial membrane and promoting the formation of bacterial biofilm[62]。 Finally,the performance of PFP-Shewanella oneidensis MR-1 hybrid was improved by 2 times when it was used for bioelectricity generation,and the current of fumarate bioelectricity synthesis of succinate was increased by 18 times(Fig.5A).Bazan et al.Studied the process by which conjugated polymers enhance bidirectional EET by forming self-assembled coatings on individual bacteria[50]。 the n-type conjugated polymer p(cNDI-gT2)with quaternary ammonium cation side chain can be wrapped on the outer membrane of Shewanella with electronegativity through electrostatic interaction.Due to the wide reduction potential,the n-type conjugated polymer p(cNDI-gT2)can simultaneously meet the reduction potential higher than the redox potential of the outward EET of Shewanella and lower than the redox potential of the inward EET of Shewanella,so that it can act as both an electron acceptor and an electron donor,thereby enhancing the bacterial bidirectional EET.This resulted in a 6-fold increase in biocurrent when the hybrid was used for bioelectricity generation and a 35-fold increase in current when fumarate was used for bioelectricity synthesis of succinate(fig.5B)。
图5 导电聚合物加速电子传递强化微生物电合成：（a）PFP包裹的希瓦氏菌MR-1促进电子摄入强化微生物电合成[62]；（b）杂合体中聚合物设计策略强化双向EET[50]

Fig. 5 Conductive polymers for accelerated electron transfer and enhanced microbial electrosynthesis. (a) PFP-coated Shewanella oneidensis MR-1 with enhanced microbial electrosynthesis through inward electron uptake[62]; Copyright 2023, Elsevier. (b) Polymer design strategy in biohybrids to enhance bidirectional EET[50]. Copyright 2023, Wiley-VCH

By constructing the conducting polymer-microorganism hybrid,the transfer rate of electrons between the microorganism and the electrode is enhanced,which helps to improve the performance of microbial electrosynthesis.In microbial electrosynthesis systems,electroactive microorganisms can directly or indirectly use electrons introduced from electrodes to fix CO2through Calvin cycle or reductive tricarboxylic acid cycle pathways to produce acids and alcohols[84]。 Although great progress has been made in microbial electrosynthesis in recent years,further research is still needed to further improve its power density。

3.3 Tabilizing cell activity and enhancing microbial chemical transformation

microorganisms can be used as green catalysts to catalyze biomass conversion sustainably.the delicate metabolic pathway of microorganisms provides a new method for the synthesis of various target compounds under mild conditions.At the same time,microorganisms have the ability of self-replication,self-protection and self-regulation,and have more advantages in stress resistance and stability than enzyme systems.With the progress of biotechnology such as synthetic biology,microbial cell factories have been developed rapidly,and have been widely concerned and applied in the production of biofuels,fine chemicals,pharmaceuticals and functional materials[12]。
microbial cells are coated with polymers,which can stabilize microbial activity under complex conditions and help microbial catalysis.Su Baolian et al.Used PDA to self-assemble on the surface of whole-cell catalyst Rhodotorula glutinis to form PDA nano-coating[35]。 the PDA coating was able to improve the cell stability of Rhodotorula glutinis,allowing the whole-cell biocatalyst to exhibit good catalytic activity and reusability in asymmetric reduction(catalytic activity was 8-fold higher than that of native cells after five cycles)(Figure 6A).Wu et al.Wrapped PDA on the surface of recombinant Escherichia coli and developed a whole-cell catalyst for multifunctional synthesis[52]。 PDA can help E.coli to resist the influence of ultraviolet light,high temperature,organic solvent and organic-water two-phase interfacial tension,and maintain the metabolic activity of bacteria.Because E.coli can express a variety of enzymes at high levels,PDA can stabilize the metabolic activity of E.coli,which is helpful for E.coli to better carry out single-enzyme,multi-enzyme and chemo-enzyme coupled catalytic reactions.in addition,the PDA coating keeps the microbial cells stable In the water-organic two-phase,allowing the whole-cell catalyst to make full use of the catalytic reaction space at the emulsion interface to achieve efficient interfacial biocatalysis(Fig.6B)。
图6 聚合物稳定细胞活性强化微生物化学转化：（a）PDA包裹的黏红酵母显示出高的催化循环稳定性[35]；（b）PDA包裹的大肠杆菌显示出高的乳液界面生物催化性能[52]；（c）PDADMAC/SiO2纳米颗粒包裹的大肠杆菌在不同温度下显示出随着涂层厚度变化而变化的生物催化性能[34]

Fig. 6 Polymer-stabilized cells with enhanced biocatalytic chemical transformation. (a) PDA-coated Rhodotorula glutinis with high cycle catalytic stability[35]; Copyright 2017, RSC. (b) PDA-coated Escherichia coli with high biocatalytic performance at the emulsion interface[52]; Copyright 2022, Springer Nature. (c) PDADMAC/SiO2 coated Escherichia coli with enhanced biocatalytic performance that varied with coating thickness at different temperatures[34]. Copyright 2019, Springer Nature

the polymer can also be Used as an interfacial layer to couple other functional materials on the surface of microorganisms.Qu et al.used PAH and PSS to biomineralize on the surface of Alcaligenes faecalis to form a calcium phosphide mineral layer doped with ferroferric oxide nanoparticles[73]。 the mineral layer enables the microbial catalyst to withstand prolonged organic solvent stress,allowing it to maintain high selectivity and cell viability after up to 30 catalytic reaction cycles.At the same time,because the doped ferroferric oxide nanoparticles have magnetism,the remote magnetic field can be Used to easily achieve in situ product separation and biocatalyst recovery.Aksan et al.used E.Coli as a model biocatalyst,coating its surface with multiple layers of oppositely charged PDADMAC and silica nanoparticles to make the microbial catalyst resistant to desiccation,freeze-thaw,high temperature exposure,osmotic shock,as well as lysozyme attack and predation by protozoa[34]。 at the same time,the silica nanoparticles can increase the permeability of the outer membrane of the biocatalyst,and the rate of the reaction of converting 3,4-dihydroxyphenylacetic acid intoα-hydroxy-δ-carboxymethyl cis-semialdehyde is increased by 2 times.the introduction of a functional coating on the surface greatly enhanced the stability of the biocatalyst,enabling it to operate At a high temperature of 60°C and further increasing the reaction rate by a factor of 21(Fig.6C)。
At present,microorganisms have become an important production route for some chemicals and pharmaceuticals.However,the application of biocatalyst is limited due to its fragile characteristics.the construction of polymer-microorganism hybrids,in which polymers or other functional materials bonded by polymers are used as protective layers of microorganisms,is helpful for the continuous and stable operation of chemical transformations involving microorganisms in complex systems,and can also endow biocatalysts with some special properties,thus broadening the application space of biocatalysis[35,43,73]。 Although many achievements have been made in the field of whole-cell biocatalysis,the quality and characteristics of engineered strains are not completely controllable,and microbial cell factories still face challenges such as unstable fermentation system,low mass transfer efficiency,low product yield and difficult separation[88,89]。 Therefore,it is essential to systematically design and develop new technologies and strategies to improve microbial production。

4 Conclusion and prospect

Coupling the physical and chemical properties of polymer materials with the biosynthetic functions of microorganisms to construct hybrids can enhance microbial catalysis,which can be used to produce fuels,chemicals,functional materials,etc.,and store green renewable energy such as solar energy in the form of chemical energy.in this paper,the construction of different types of polymer-microorganism hybrids is systematically summarized,and the improvement of biocatalytic performance of polymer-microorganism hybrids is reviewed in detail from three aspects:enhancing light energy utilization,accelerating electron transfer,and stabilizing biological activity.the systematic design of the hybrid system is helpful to further improve its catalytic performance and expand its application scenarios。
First of all,the systematic design of microorganisms and polymer materials can improve the physical,chemical and biological compatibility between them.Natural microorganisms are modified and screened by modern synthetic biology methods to better adapt to the photoelectric characteristics of polymer materials and the synthesis of target products.at the same time,the size,morphology and composition of the polymer were controlled to enhance its matching with microorganisms.the study of energy transfer mechanism can guide the design of functional polymer-microorganism hybrid system.Spectroscopic techniques such as transient absorption spectroscopy,Raman spectroscopy and Fourier transform infrared spectroscopy can be used to analyze the material and energy transfer process At the polymer-microorganism hybrid interface,so as to explore the influence mechanism of different hybrid interface structures on the energy transfer mechanism and biological metabolic pathway。
Secondly,the mass transfer of the reaction substrate at the microbial interface In the microbial catalytic reaction system was optimized.the polymer coating on the surface of microorganisms may affect the contact of microorganisms with reaction substrates,the uptake and excretion of nutrients and metabolites,reduce the efficiency of biocatalysis and affect life activities such as microbial reproduction.Therefore,it is necessary to enhance the mass transfer at the polymer interface during the construction of polymer-microorganism hybrids.polymer coatings with reversible adhesion to microbial cells can be designed to achieve controlled mass and energy transfer.in addition,the coverage,thickness and porosity of the polymer material on the surface of the microorganism can be regulated,or the polymer-microorganism hybrid can be constructed on the surface of the microorganism by using the polymer micro-nanoparticle。
Finally,functional polymer-microbial hybrids have shown advantages in the fields of semi-artificial photosynthesis,bioelectrosynthesis and interfacial catalysis,and have great potential applications in the fixation and conversion of CO2,the storage and release of electrical energy,and the production of fuels and chemicals.However,the large-scale cultivation and application of hybrids also face problems such as low energy conversion efficiency,high cost of polymer materials,insufficient long-term stability and difficult compatibility with bioreactors.In the follow-up research,it is necessary to develop cheap and efficient functional polymer materials and evaluate their long-term stability in the biocatalytic reaction system,and also to develop bioreactors suitable for hybrid catalytic reactions and explore the prospects of their large-scale application 。
At present,the research on the hybrid system of functional materials and microorganisms,especially the polymer-microorganism hybrid,is still in its infancy.with the continuous development of materials,chemistry and biology,as well as the in-depth exploration of researchers in this field,it is believed that more functional material-microbial hybrid systems With application potential will be developed in the future。

References

Publishing order | Descend order by publishing year | Descend order by cited within
[1]
Nelson N, Ben-Shem A. Nat. Rev. Mol. Cell Biol., 2004, 5(12): 971.

[2]
Jia C C, Kan X N, Zhang X, Lin G, Liu W G, Wang Z Y, Zhu S Q, Ju D X, Liu J. Chem. Eng. J., 2022, 427: 131554.

[3]
Liu J, Antonietti M. Energy Environ. Sci., 2013, 6(5): 1486.

[4]
Liu W G, Hu W J, Yang L J, Liu J. Nano Energy, 2020, 73: 104750.

[5]
Seh Z W, Kibsgaard J, Dickens C F, Chorkendorff I, Nørskov J K, Jaramillo T F. Science, 2017, 355(6321): eaad4998.

[6]
Ross M B, De Luna P, Li Y F, Dinh C T, Kim D, Yang P D, Sargent E H. Nat. Catal., 2019, 2(8): 648.

[7]
Shan X Y, Liu J, Mu H R, Xiao Y, Mei B B, Liu W G, Lin G, Jiang Z, Wen L P, Jiang L. Angew. Chem. Int. Ed., 2020, 59(4): 1659.

[8]
Cestellos-Blanco S, Zhang H, Kim J M, Shen Y X, Yang P D. Nat. Catal., 2020, 3(3): 245.

[9]
Bell E L, Finnigan W, France S P, Green A P, Hayes M A, Hepworth L J, Lovelock S L, Niikura H, Osuna S, Romero E, Ryan K S, Turner N J, Flitsch S L. Nat. Rev. Meth. Primers, 2021, 1: 46.

[10]
Miller D C, Athavale S V, Arnold F H. Nat. Synth., 2022, 1(1): 18.

[11]
Kornienko N, Zhang J Z, Sakimoto K K, Yang P D, Reisner E. Nat. Nanotechnol., 2018, 13(10): 890.

[12]
Ko Y S, Kim J W, Lee J A, Han T, Kim G B, Park J E, Lee S Y. Chem. Soc. Rev., 2020, 49(14): 4615.

[13]
Liu Z H, Wang K, Chen Y, Tan T W, Nielsen J. Nat. Catal., 2020, 3(3): 274.

[14]
Lubitz W, Ogata H, Rüdiger O, Reijerse E. Chem. Rev., 2014, 114(8): 4081.

[15]
Zhang S W, Heyes D J, Feng L L, Sun W L, Johannissen L O, Liu H T, Levy C W, Li X M, Yang J, Yu X L, Lin M, Hardman S J O, Hoeven R, Sakuma M, Hay S, Leys D, Rao Z H, Zhou A W, Cheng Q, Scrutton N S. Nature, 2019, 574(7780): 722.

[16]
Tang T C, An B L, Huang Y Y, Vasikaran S, Wang Y Y, Jiang X Y, Lu T K, Zhong C. Nat. Rev. Mater., 2021, 6(4): 332.

[17]
Lin G, Zhang Y Y, Hua Y T, Zhang C H, Jia C C, Ju D X, Yu C M, Li P, Liu J. Angew. Chem. Int. Ed., 2022, 61: e202206283.

[18]
Atsumi S, Higashide W, Liao J C. Nat. Biotechnol., 2009, 27(12): 1177.

[19]
Liew F E, Nogle R, Abdalla T, Rasor B J, Canter C, Jensen R O, Wang L, Strutz J, Chirania P, De Tissera S, Mueller A P, Ruan Z H, Gao A, Tran L, Engle N L, Bromley J C, Daniell J, Conrado R, Tschaplinski T J, Giannone R J, Hettich R L, Karim A S, Simpson S D, Brown S D, Leang C, Jewett M C, Köpke M. Nat. Biotechnol., 2022, 40(3): 335.

[20]
Ro D K, Paradise E M, Ouellet M, Fisher K J, Newman K L, Ndungu J M, Ho K A, Eachus R A, Ham T S, Kirby J, Chang M C Y, Withers S T, Shiba Y, Sarpong R, Keasling J D. Nature, 2006, 440(7086): 940.

[21]
Sakimoto K K, Wong A B, Yang P D. Science, 2016, 351(6268): 74.

[22]
Hu G P, Li Z H, Ma D L, Ye C, Zhang L P, Gao C, Liu L M, Chen X L. Nat. Catal., 2021, 4(5): 395.

[23]
Wang X Y, Zhang J C, Li K, An B L, Wang Y Y, Zhong C. Sci. Adv., 2022, 8(18): eabm7665.

[24]
Ye J, Wang C, Gao C, Fu T, Yang C H, Ren G P, Lü J, Zhou S G, Xiong Y J. Nat. Commun., 2022, 13: 6612.

[25]
Lin Y L, Shi J Y, Feng W, Yue J P, Luo Y Q, Chen S, Yang B, Jiang Y W, Hu H C, Zhou C K, Shi F Y, Prominski A, Talapin D V, Xiong W, Gao X, Tian B Z. Sci. Adv., 2023, 9(29): eadg5858.

[26]
Yu W, Zeng Y, Wang Z H, Xia S P, Yang Z W, Chen W J, Huang Y M, Lv F T, Bai H T, Wang S. Sci. Adv., 2023, 9(11): eadf6772.

[27]
Cao B C, Zhao Z P, Peng L L, Shiu H Y, Ding M N, Song F, Guan X, Lee C K, Huang J, Zhu D, Fu X Y, Wong G C L, Liu C, Nealson K, Weiss P S, Duan X F, Huang Y. Science, 2021, 373(6561): 1336.

[28]
Yu Y Y, Wang Y Z, Fang Z, Shi Y T, Cheng Q W, Chen Y X, Shi W D, Yong Y C. Nat. Commun., 2020, 11: 4087.

[29]
Song R B, Wu Y C, Lin Z Q, Xie J, Tan C H, Loo J S C, Cao B, Zhang J R, Zhu J J, Zhang Q C. Angew. Chem. Int. Ed., 2017, 56(35): 10516.

[30]
Wang R W, Li H D, Sun J Z, Zhang L, Jiao J, Wang Q Q, Liu S Q. Adv. Mater., 2021, 33: 2004051.

[31]
Xiong W, Zhao X H, Zhu G X, Shao C Y, Li Y L, Ma W M, Xu X R, Tang R K. Angew. Chem. Int. Ed., 2015, 54(41): 11961.

[32]
Su D Y, Qi J R, Liu X M, Wang L, Zhang H, Xie H, Huang X. Angew. Chem. Int. Ed., 2019, 58(12): 3992.

[33]
Xu Z J, Qi J R, Wang S L, Liu X M, Li M, Mann S, Huang X. Nat. Commun., 2023, 14: 1872.

[34]
Sakkos J K, Wackett L P, Aksan A. Sci. Rep., 2019, 9: 3158.

[35]
Wang L, Hu Z Y, Yang X Y, Zhang B B, Geng W, Van Tendeloo G, Su B L. Chem. Commun., 2017, 53(49): 6617.

[36]
Wang W S, Wang S T. Lab a Chip, 2022, 22(6): 1042.

[37]
Pan C, Li J J, Hou W L, Lin S S, Wang L, Pang Y, Wang Y F, Liu J Y. Adv. Mater., 2021, 33(13): 2007379.

[38]
Niu J, Lunn D J, Pusuluri A, Yoo J I, O’Malley M A, Mitragotri S, Soh H T, Hawker C J. Nat. Chem., 2017, 9(6): 537.

[39]
Geng J, Li W S, Zhang Y C, Thottappillil N, Clavadetscher J, Lilienkampf A, Bradley M. Nat. Chem., 2019, 11(6): 578.

[40]
Lin J C, Chien C Y, Lin C L, Yao B Y, Chen Y I, Liu Y H, Fang Z S, Chen J Y, Chen W Y, Lee N N, Chen H W, Hu C M J. Nat. Commun., 2019, 10: 1057.

[41]
Yang S H, Ko E H, Jung Y H, Choi I S. Angew. Chem. Int. Ed., 2011, 50(27): 6115.

[42]
Wang W S, Gan Q, Zhang Y Q, Lu X, Wang H X, Zhang Y K, Hu H, Chen L N, Shi L X, Wang S T, Zheng Z J. Adv. Mater., 2021, 33(34): 2102348.

[43]
Guo J L, Suástegui M, Sakimoto K K, Moody V M, Xiao G, Nocera D G, Joshi N S. Science, 2018, 362(6416): 813.

[44]
Lin J C, Hsu C Y, Chen J Y, Fang Z S, Chen H W, Yao B Y, Shiau G H M, Tsai J S, Gu M, Jung M, Lee T Y, Hu C M J. Adv. Mater., 2021, 33: 2101190.

[45]
Liu J, Kim Y S, Richardson C E, Tom A, Ramakrishnan C, Birey F, Katsumata T, Chen S C, Wang C, Wang X, Joubert L M, Jiang Y W, Wang H L, Fenno L E, Tok J B H, Pașca S P, Shen K, Bao Z N, Deisseroth K. Science, 2020, 367(6484): 1372.

[46]
Sessler C D, Zhou Y M, Wang W B, Hartley N D, Fu Z Y, Graykowski D, Sheng M, Wang X, Liu J. Sci. Adv., 2022, 8(49): eade1136.

[47]
Gai P P, Yu W, Zhao H, Qi R L, Li F, Liu L B, Lv F T, Wang S. Angew. Chem. Int. Ed., 2020, 59(18): 7224.

[48]
Zeng Y, Zhou X, Qi R L, Dai N, Fu X C, Zhao H, Peng K, Yuan H T, Huang Y M, Lv F T, Liu L B, Wang S. Adv. Funct. Mater., 2021, 31(8): 2007814.

[49]
Zeng Y, Bai H T, Yu W, Xia S P, Shen Q, Huang Y M, Lv F T, Bazan G C, Wang S. Angew. Chem. Int. Ed., 2023, 60: e202303877.

[50]
Quek G, McCuskey S R, Vázquez R J, Cox-Vázquez S J, Bazan G C. Adv. Electron. Mater., 2023, 9(7): 2370035.

[51]
Du Q, Li T, Li N, Wang X. Environ. Sci. Technol. Lett., 2017, 4(8): 345.

[52]
Sun Z Y, Hübner R, Li J, Wu C Z. Nat. Commun., 2022, 13: 3142.

[53]
Ding L, Yu Z D, Wang X Y, Yao Z F, Lu Y, Yang C Y, Wang J Y, Pei J. Chem. Rev., 2023, 123(12): 7421.

[54]
Zeglio E, Rutz A L, Winkler T E, Malliaras G G, Herland A. Adv. Mater., 2019, 31(22): 1806712.

[55]
Zhou X, Zeng Y, Tang Y Y, Huang Y M, Lv F T, Liu L B, Wang S. Sci. Adv., 2020, 6(35): eabc5237.

[56]
Qi R L, Zhao H, Zhou X, Liu J, Dai N, Zeng Y, Zhang E D, Lv F T, Huang Y M, Liu L B, Wang Y L, Wang S. Angew. Chem. Int. Ed., 2021, 60(11): 5759.

[57]
Xu M Y, Tremblay P L, Jiang L L, Zhang T. Green Chem., 2019, 21(9): 2392.

[58]
Tremblay P L, Xu M Y, Chen Y M, Zhang T. iScience, 2020, 23(1): 100784.

[59]
Ye J, Chen Y P, Gao C, Wang C, Hu A D, Dong G W, Chen Z, Zhou S G, Xiong Y J. Angew. Chem. Int. Ed., 2022, 61(52): e202217507.

[60]
Sheng Y K, Guo F, Guo B C, Wang N, Sun Y Y, Liu H, Feng X D, Han Q, Yu Y, Li C. ACS Synth. Biol., 2023, 12(9): 2715.

[61]
Wu D, Zhang W M, Fu B H, Zhang Z H. Joule, 2022, 6(10): 2293.

[62]
Zhang P B, Zhou X, Wang X Y, Li Z P. Colloids Surf. B Biointerfaces, 2023, 228: 113383.

[63]
Luo H P, Qi J X, Zhou M Z, Liu G L, Lu Y B, Zhang R D, Zeng C P. Bioresour. Technol., 2020, 309: 123322.

[64]
Wang Z J, Gao D, Zhan Y, Xing C F. ACS Appl. Bio Mater., 2020, 3(5): 3423.

[65]
Yu W, Pavliuk M V, Liu A J, Zeng Y, Xia S P, Huang Y M, Bai H T, Lv F T, Tian H N, Wang S. ACS Appl. Mater. Interfaces, 2023, 15(1): 2183.

[66]
Yu W, Bai H T, Zeng Y, Zhao H, Xia S P, Huang Y M, Lv F T, Wang S. Research, 2022, 2022: 9834093.

[67]
Wang D L, Pan J Y, Xu M, Liu B C, Hu J P, Hu S G, Hou H J, Elmaadawy K, Yang J K, Xiao K K, Liang S. J. Power Sources, 2021, 483: 229220.

[68]
Zhou X, Zeng Y, Lv F T, Bai H T, Wang S. Acc. Chem. Res., 2022, 55(2): 156.

[69]
Driks A. Trends Microbiol., 2002, 10(6): 251.

[70]
Hildebrand M. Chem. Rev., 2008, 108(11): 4855.

[71]
Hong D, Park M, Yang S H, Lee J, Kim Y G, Choi I S. Trends Biotechnol., 2013, 31(8): 442.

[72]
Lei Q, Guo J M, Kong F H, Cao J F, Wang L, Zhu W, Brinker C J. J. Am. Chem. Soc., 2021, 143(17): 6305.

[73]
Chen Z W, Ji H W, Zhao C Q, Ju E G, Ren J S, Qu X G. Angew. Chem. Int. Ed., 2015, 54(16): 4904.

[74]
Wei W, Sun P Q, Li Z, Song K S, Su W Y, Wang B, Liu Y Z, Zhao J. Sci. Adv., 2018, 4(2): eaap9253.

[75]
Konnova S A, Lvov Y M, Fakhrullin R F. Langmuir, 2016, 32(47): 12552.

[76]
Lee H, Dellatore S M, Miller W M, Messersmith P B. Science, 2007, 318(5849): 426.

[77]
Guo J L, Tardy B L, Christofferson A J, Dai Y L, Richardson J J, Zhu W, Hu M, Ju Y, Cui J W, Dagastine R R, Yarovsky I, Caruso F. Nat. Nanotechnol., 2016, 11(12): 1105.

[78]
Blankenship R E, Tiede D M, Barber J, Brudvig G W, Fleming G, Ghirardi M, Gunner M R, Junge W, Kramer D M, Melis A, Moore T A, Moser C C, Nocera D G, Nozik A J, Ort D R, Parson W W, Prince R C, Sayre R T. Science, 2011, 332(6031): 805.

[79]
Galloway J N, Townsend A R, Erisman J W, Bekunda M, Cai Z C, Freney J R, Martinelli L A, Seitzinger S P, Sutton M A. Science, 2008, 320(5878): 889.

[80]
Tan C L, Xu P, Tao F. Trends Biotechnol., 2022, 40(12): 1488.

[81]
Zhang S S, Sun J H, Feng D D, Sun H L, Cui J Y, Zeng X X, Wu Y N, Luan G D, Lu X F. Nat. Commun., 2023, 14: 3425.

[82]
Kumar A, Hsu L H H, Kavanagh P, Barrière F, Lens P N L, Lapinsonnière L, Lienhard V J H, Schröder U, Jiang X C, Leech D. Nat. Rev. Chem., 2017, 1(3): 24.

[83]
Rabaey K, Rozendal R A. Nat. Rev. Microbiol., 2010, 8(10): 706.

[84]
Fang Z, Tang Y J, Koffas M A. Curr. Opin. Biotechnol., 2022, 75: 102687.

[85]
Zhang T, Nie H R, Bain T S, Lu H Y, Cui M M, Snoeyenbos-West O L, Franks A E, Nevin K P, Russell T P, Lovley D R. Energy Environ. Sci., 2013, 6(1): 217.

[86]
Kaneko M, Ishihara K, Nakanishi S. Small, 2020, 16(34): 2001849.

[87]
McCuskey S R, Su Y D, Leifert D, Moreland A S, Bazan G C. Adv. Mater., 2020, 32(24): 2070181.

[88]
Rugbjerg P, Sommer M O A. Nat. Biotechnol., 2019, 37(8): 869.

[89]
Wehrs M, Tanjore D, Eng T, Lievense J, Pray T R, Mukhopadhyay A. Trends Microbiol., 2019, 27(6): 524.

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